Non-canonical dorsoventral patterning in the moth midge Clogmia albipunctata

Karl R Wotton,Anna Alcaine-Colet,Johannes Jaeger,Eva Jiménez-Guri

doi:10.1186/s13227-017-0083-9

Abstract

BackgroundBone morphogenetic proteins (BMPs) are of central importance for dorsal–ventral (DV) axis specification. They are core components of a signalling cascade that includes the BMP ligand decapentaplegic (DPP) and its antagonist short gastrulation (SOG) in Drosophila melanogaster. These components are very ancient, with orthologs involved in DV patterning in both protostomes and deuterostomes. Despite such strong conservation, recent comparative work in insects has revealed interesting differences in the way the patterning function of the DV system is achieved in different species.ResultsIn this paper, we characterise the expression patterns of the principal components of the BMP DV patterning system, as well as its signalling outputs and downstream targets, in the non-cyclorrhaphan moth midge Clogmia albipunctata (Diptera: Psychodidae). We previously reported ventral expression patterns of dpp in the pole regions of C. albipunctata blastoderm embryos. Strikingly, we also find ventral sog and posteriorly restricted tkv expression, as well as expanded polar activity of pMad. We use our results from gene knock-down by embryonic RNA interference to propose a mechanism of polar morphogen shuttling in C. albipunctata. We compare these results to available data from other species and discuss scenarios for the evolution of DV signalling in the holometabolan insects.ConclusionsA comparison of gene expression patterns across hemipteran and holometabolan insects reveals that expression of upstream signalling factors in the DV system is very variable, while signalling output is highly conserved. This has two major implications: first, as long as ligand shuttling and other upstream regulatory mechanisms lead to an appropriately localised activation of BMP signalling at the dorsal midline, it is of less importance exactly where the upstream components of the DV system are expressed. This, in turn, explains why the early-acting components of the DV patterning system in insects exhibit extensive amounts of developmental systems drift constrained by highly conserved downstream signalling output.

Highlights

Bone morphogenetic proteins (BMPs) are of central importance for dorsal–ventral (DV) axis specifica‐ tion
Expression patterns of the DV patterning system components and its downstream targets in C. albipunctata We examined the expression patterns of the major components of the BMP signalling cascade comprising the DV patterning system as well as its core signalling output and key downstream targets in blastoderm and postgastrulation embryos of the moth midge C. albipunctata
Our results and other work on BMP DV patterning in insects [3, 5, 20,21,22,23,24,25, 55] reveal that BMP ligands, as well as other factors involved in their transport, can be expressed at many different positions along the DV axis in different insect species (Fig. 6)

Summary

Introduction

Bone morphogenetic proteins (BMPs) are of central importance for dorsal–ventral (DV) axis specifica‐ tion They are core components of a signalling cascade that includes the BMP ligand decapentaplegic (DPP) and its antagonist short gastrulation (SOG) in Drosophila melanogaster. Signalling molecules of the TGF-β family are widely conserved across the animal kingdom They are key factors in developmental processes such as dorsal–ventral (DV) axis specification, appendage formation, patterning of the central nervous system, and cell proliferation (reviewed in [1]). The resulting free ligand dimers attach to their receptors [encoded by punt (put), saxophone (sax), and thick veins (tkv)], which form transmembrane complexes [9, 12] (Fig. 1c) This binding event triggers an intracellular signalling process: once the ligand–receptor complex has been established, SAX and TKV phosphorylate Mothers against dpp (MAD). In the DV patterning system, initially triggered by the Toll signalling pathway [13, 14], dpp is a key factor for the determination of dorsal tissues and acts as a morphogen for the specification of the dorsal ectoderm and the amnioserosa [6, 15]; see [9, 10] for a review

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